BASIC AND CLINICAL ASPECTS OF VERTIGO AND DIZZINESS
Perceptual Encoding of Self-Motion Duration in Human Posterior Parietal Cortex Barry M. Seemungal,a Vincenzo Rizzo,b Michael A. Gresty,a John C. Rothwell,b and Adolfo M. Bronsteina a
Neuro-Otology Unit, Division of Neuroscience, Charing Cross Hospital, Imperial College, London, UK b
Sobell Department of Motor Neuroscience and Movement Disorders, Institute of Neurology, UCL, London, UK
It has been demonstrated previously that repetitive transcranial magnetic stimulation (rTMS) to right or left posterior parietal cortex (PPC) disrupts perceptual encoding of whole-body displacement during an angular path integration task using only vestibular cues for its completion. The effects of rTMS applied to right PPC (and left motor cortex as a control) during a vestibular-cued motion-reproduction task (i.e., not requiring path integration) were investigated in 5 subjects. Specifically, subjects were rotated in the ´ any ´ dark on a motorized Bar chair with raised cosine velocities of durations 1, 2, and 3 s and peak 30◦ , 60◦ , 90◦ , and 120◦ /s. Subjects were required to actively reproduce the motion profile after every rotation with a chair-bound joystick. It was found that rTMS applied to the right PPC during the passive (encoding) stimulus phase had no effect on angular velocity reproduction when compared to control (motor-cortex rTMS). In contrast, motion-duration reproduction was significantly worse with right PPC (versus control motor cortex) rTMS. The results imply that vestibular-derived cues of motion duration, but not velocity, are encoded in human PPC. It was inferred from these and previous data that human PPC is involved in human path integration and motionduration perception, but not angular velocity self-motion perception. Key words: vestibular perception; time perception; vestibular navigation; vestibular cortex; parietal cortex; repetitive transcranial magnetic stimulation; rTMS; memory
During everyday locomotion, multisensory input generates perceptions of motion and position-in-space, and in the dark, these perceptions become reliant upon vestibular input, particularly during locomotor turning.1 Navigation tasks that isolate vestibular input, called “vestibular navigation,” have demonstrated that humans can orient using only vestibular signals1–3 (see also Fig. 1), implying a temporal integration of the vestibular signal of angular head velocity to provide the complementary perception of change in spatial
Address for correspondence: Barry M. Seemungal, Division of Neuroscience, Charing Cross Hospital, Imperial College, London W6 8RF, UK.
[email protected]
orientation. Vestibular navigation paradigms can be performed by path integration—when subjects are required to update angular displacement; or self-motion reproduction— when subjects are required to reproduce the velocity profile of self-motion (compare Fig. 1B with 1C). We have shown that during human angular-path integration, right or left posterior parietal cortex (PPC) encodes contralaterally directed passive angular rotations;1 for example, left hemisphere encodes rightward angular displacements. But what of vestibularly sensed angular velocity and motion-duration encoding? We used repetitive transcranial magnetic stimulation (rTMS) to transiently disrupt focal cortical function in a vestibular navigation
Basic and Clinical Aspects of Vertigo and Dizziness: Ann. N.Y. Acad. Sci. 1164: 236–238 (2009). C 2009 New York Academy of Sciences. doi: 10.1111/j.1749-6632.2009.03772.x
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Seemungal et al.: Self-motion Duration Perception in Parietal Cortex
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Figure 2. The main results. This figure shows the unsigned percentage error of response for peak velocity and motion duration for both motor and parietal cortex rTMS.
Figure 1. Apparatus and representative angular chair velocity recordings. (A) Top left panel shows the motorized rotating chair with joystick control and headphones delivering white-noise sound masking. Top right panel shows the mounted TMS coil. (B) Representative chair angular velocity trace during velocity-matching strategy, showing a rightward (upward deflection) stimulus rotation of “raised cosine” waveform, followed by a leftward rotation response of similar shape to the stimulus. (C) For comparison, a displacement-matching strategy is shown (not required in the current experiment) where the response profile is trapezoidal.
task involving whole-body rotations, adapted to separately study vestibular-derived displacement versus velocity perception.1 Briefly, subjects were passively rotated (without vision or audition) on a motorized “B´ar´any chair” from a start position, and were required to return themselves to start using only vestibular signals for guidance (Fig. 1—the “self-rotation test”). In the results that we report here, subjects were told to reproduce the kinetics (angular velocity
and motion duration) of the stimulus rotation (Fig. 1B). Correlations between response and stimulus for peak angular velocity (r 2 = 0.58; n = 440 trials for 5 subjects for both PPC and motor-cortex conditions combined), and motion duration (r 2 = 0.60; n = 440) confirmed subjects’ compliance with instructions to match stimulus kinetics. We applied rTMS during the passive phase to right PPC or left motor cortex (see Ref. 1 for rTMS parameters). We found no difference in% error of response of peak angular velocity reproduction when rTMS was applied to right PPC or motor cortex for rightward and leftward stimulus rotations combined (Fig. 2, right). In contrast, % error of motion-duration response was significantly worse (P = 0.028; paired t-test: n = 220) for parietal versus motor rTMS (Fig. 2, left). We further analyzed the directional effect of rTMS on motion-duration response (i.e., by analyzing responses for rightward and leftward stimulus rotations separately) by repeated-measures ANOVA with factors: locus of rTMS (parietal vs. motor) and stimulus rotation displacement direction (right vs. left). There was a significant effect of locus of rTMS (F[1,109] = 16.12, P < 0.0001) and stimulus rotational direction
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(F [1,109] = 7.98, P = 0.006) with a significant interaction between stimulus direction and rTMS location (F [1,109] = 4.61, P = 0.03). Two post hoc paired t-test comparisons confirmed a significant response asymmetry (rightward vs. leftward stimuli) during right parietal cortex rTMS (P = 0.001), but not during motor cortex rTMS (P = 0.47). Specifically, right parietal rTMS (under kinetic-matching conditions) impaired encoding of motion duration for ipsilaterally directed rotations; this is in contrast to the contralateral effect we have previously seen for parietal rTMS on angular displacement encoding during path integration, that is, under displacement-matching conditions.1 Our results suggest that human PPC may be considered “secondary” vestibular cortex since it is involved in the perceptual encoding of secondary vestibular signals of angular displacement1 and motion duration, but not primary vestibular signals of angular velocity.
Annals of the New York Academy of Sciences Conflicts of Interest
The authors declare no conflicts of interest. References 1. Seemungal, B.M., V. Rizzo, M.A. Gresty, et al. 2008. Posterior parietal rTMS disrupts human path integration during a vestibular navigation task. Neurosci. Lett. 437: 88–92. 2. Glasauer, S., M.A. Amorim, I. Viaud-Delmon & A. Berthoz. 2002. Differential effects of labyrinthine dysfunction on distance and direction during blindfolded walking of a triangular path. Exp. Brain Res. 145: 489– 497. 3. Metcalfe, T. & M. Gresty. 1992. Self-controlled reorienting movements in response to rotational displacements in normal subjects and patients with labyrinthine disease. Ann. N.Y. Acad. Sci. 656: 695– 698. 4. Seemungal, B.M., S. Glasauer, M.A. Gresty & A.M. Bronstein. 2007. Vestibular perception and navigation in the congenitally blind. J. Neurophysiol. 97: 4341– 4356.
